The first three paragraphs of Jane Peterson’s contribution to the Second Anolis Newsletter.
Jane Peterson’s contribution to The Second Anolis Newsletter remains one of the most comprehensive exemplars of functional-morphological research of the anoline appendicular girdles. In just a few short paragraphs Peterson (1974) outlined the key differences in pectoral girdle morphology between the Anolis ecomorphs, drawing information from both field observations and anatomical dissections of anoles from all four Greater Antillean islands. The outlined study could have formed a major contribution to our understanding of ecomorphology, had these brief observations ever been expanded into a scientific publication. Sadly, they remained as notes, confined to a brief communique on an informal basis (that continues to be formally cited). Several intriguing studies hence have examined anole appendicular morphology, but rarely allowed for implications that reach across multiple island radiations (e.g. Anzai et al. 2014, Herrel et al. 2018).
With my 2016 Ph.D. thesis, I set out to quantify what Jane Peterson had observed forty years prior, and must confess that I still fall short of reproducing the multitude of implications that Peterson’s (1974) brief descriptions alluded to. Instead of combining video-recorded movement cycles with morphological descriptions, my comparisons are solely based on three-dimensional shape analysis of the skeletal elements that comprise the breast-shoulder apparatus (BSA): the clavicle, interclavicle, presternum, and scapulocoracoid (Fig. 1). Employing the power of computed tomography scanning, and geometric morphometric analysis, I quantified the shapes of the central elements of the pectoral girdle, and compared these across anole radiations.
As with earlier work, I focused on the Jamaican ecomorph representatives, and sought out their ecomorph counterparts from Hispaniola and Puerto Rico, particularly targeting those species that are the most and least similar to the Jamaican forms. That last line of thought did not reveal any straightforward answers, as the complex structural shape of the BSA allows these anoles to be relatively distinct in some aspects, while being quite similar in others. For example, the general shape of the presternum and interclavicle are quite similar between the two trunk-ground anoles Anolis lineatopus (Jamaica) and A. gundlachi (Puerto Rico), while that of the scapulocoracoid differs quite remarkably between the two. These complex associations will take a more detailed analysis than what is warranted here, so I’ll focus on the bigger picture instead.
Fig. 1: CT-rendition of the skeletal components of the breast-shoulder apparatus of Anolis baleatus in lateromedial view, depicting all anatomical features described in the text. The gray arrow denotes anterior.
Skeletal elements of the BSA in isolation
Previous analysis of the scapulocoracoid in isolation revealed that its shape differs between Anolis habitat specialists, and resembles a particularly dorsoventrally tall shape in twig anoles (Tinius et al. 2020). The other ecomorph groups (trunk-ground, trunk-crown, and crown-giant) show obvious tendencies towards a particular structural organization, but in none of these does the scapulocoracoid resemble a truly characteristic shape.
Since the presternum and interclavicle are immovably linked, we analysed these two elements as one continuous moiety. In twig anoles, this structure is of relatively great anteroposterior extent, with a posterior displacement of the articulatory facets for the sternal ribs. The whole shape of the presternum-interclavicle moiety seems to draw the muscle vectors of humeral pro-and retractors into a more horizontal orientation in twig forms, compared to other ecomorph groups.
Finally, the shape analysis of the clavicle does not show any particular pattern. Anolis species occupy distinct portions of morphospace, but neither geography, nor phylogenetic relationship, nor ecological specialisation have a distinct effect on clavicle shape. That is not to say there is no signal here. However, the biological history of this seemingly simple bone is so complex that it cannot be depicted adequately by the three landmarks that were available to us in this study. The form of the clavicle has frequently been used to provide character traits for phylogenetic analysis, and a more thorough analysis is certainly warranted.
Landmark manipulation
The focus of this study was to combine the three moieties of clavicle, presternum-interclavicle, and scapulocoracoid into one geometric structure, which is obviously a silly idea, because all these parts are mobile with respect to another. I spent countless hours manipulating those three moieties in ‘Autodesk Maya’, to achieve a standardized position of these mobile elements with respect to another. That way we were able to use geometric morphometric analysis to investigate the shape of the BSA despite the mobility of its component parts.
This process of individual bone manipulation is long and arduous, meaning it actually took a fully-funded Ph.D. project to achieve this with a meaningful sample size. I am grateful to various funding agencies and most importantly my supervisor Anthony P. Russell for providing me with the necessary resources. Recently, Rhoda et al. (2021) developed an algorithm that performs a same task of retroactive landmark reconfiguration, which nullifies the need for individual manipulation. At first, I was sceptical about the algorithm’s performance with complex articulations that stray from a simple hinge joint. However, after testing this ‘local superimposition’ method on our BSA data, and comparing the results with my manual manipulation of surface meshes, I can confirm that the results from Rhoda et al.’s (2021) algorithm work just as well.
Fig. 2: Scatter plot of the first two principal components of the in situ configuration of the breast-shoulder apparatus (BSA). The CT-renditions indicate the shape differences between the negative (left) and positive (rigth) extremes along the PC1 axis. Superimposed heat maps indicate the relative extent of shape variation in that area, ranging from major (red) to minor (blue). One specimen of Anolis baleatus was used as template for the renditions of deformation. The gray arrow denotes anterior. The blue lines indicate the extent and direction of shape difference towards the opposite extreme. Numbers in parentheses on each axis indicate the percentage of variance explained by each principal component.
The shape of the BSA
Combining all three moieties into one complex 3-D shape actually obscures much of the shape variation that is evident in the single-element analyses (Fig. 2). While the positional information of these three moieties does provide useful information that separates certain habitat specialists, it also obscures some of the variation that seems obvious when looking at the isolated presternum-interclavicle or scapulocoracoid moieties (Fig. 2). For example, the scapulocoracoid appears relatively dorsoventrally tall in twig anoles (compared to other ecomorphs), a distinction that almost vanishes in the analysis of the BSA. Instead, the dorsoventral height of the scapula interacts closely with the anteroposterior width of the epicoracoid, giving the former a relatively tall appearance.
In detail, these shape variations are fairly complex, but as Peterson (1974) alluded to, the four major ecomorph groups (trunk-ground, trunk-crown, crown-giant, and twig) all show particular morphological characteristics that relate directly to their locomotor abilities. In trunk-ground anoles, the BSA is relatively anteroposteriorly short, with a more dorsally located glenoid fossa (Figs. 2, 3). This likely shifts the muscle vectors of major humeral pro- and retractors to involve a greater component of adduction. Humeral adduction probably helps trunk-ground anoles in being acrobatic leapers that put greater emphasis on sudden jumps and manoeuvres than other ecomorph representatives.
Trunk and trunk-crown anoles seem to have a relatively featureless BSA, in which a cylindrical organisation of the skeletal components restricts their mobility (Figs. 2, 3). That also means their BSA remains relatively stable while quickly climbing in various directions. Their pectoral girdle seems to be geared towards rapid and sustained movement, at the cost of relatively lesser forelimb excursion, compared to other habitat specialists.
Twig anoles are quite peculiar, moving relatively slowly on ludicrously narrow perches. Various authors have compared their slow movements to those of chameleons, and their BSA features many of the same structural specialisations. The pectoral girdle of twig anoles is relatively lateromedially narrow, and the potential for anteroposterior displacement of the scapulocoracoid in the coracosternal groove is markedly greater than in other ecomorphs (Figs. 2, 3). This allows twig forms to adduct the humerus further than other ecomorphs, and increase their stride length through movement of the scapulocoracoid. Basically, twig anoles can make relatively long strides with relatively stubby forelimbs, thereby reaching far with their feet despite involving only minor lateral bending of the trunk, which stabilises them on narrow perches.
Fig. 3: CT-rendition of the breast-shoulder apparatus of Anolis lineatopus, A. eladioi and A. valencienni, as representatives of the trunk-ground, trunk-crown, and twig ecomorph groups, respectively. The gray arrow denotes anterior.
Conclusions
In summary, our study provides quantitative evidence for assertions that Jane Peterson (1974) made several decades ago, and still falls short of directly combining anatomical detail with live observations. However, we were able to provide a comprehensive account of the major skeletal components of the BSA of Anolis lizards, both in isolation and in situ, and directly link morphological differences between habitat specialists to their respective locomotor capabilities.
References
Anzai, W., Omura, A., Diaz, A.C., Kawata, M. & Endo, H. (2014): Functional morphology and comparative anatomy of appendicular musculature in Cuban Anolis lizards with different locomotor habits.─ Zoological Science, 31(7):454-463; DOI: http://dx.doi.org/10.2108/zs130062.
Herrel, A., Vanhooydonck, B., Porck, J. & Irschick, D.J. (2018): Anatomical basis of differences in locomotor behavior in Anolis lizards: a comparison between two ecomorphs.─ Bulletin of the Museum of Comparative Zoology, 159(4):213-238; https://doi.org/10.3099/0027-4100-159.4.213.
Peterson, J.A. (1974) [In:] Williams, E.E. (Ed.): The Second Anolis Newsletter. Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts.
Rhoda, D., Segall, M., Larouche, O., Evans, K. & Angielczyk, K.D. (2021): Local superimpositions facilitate morphometric analysis of complex articulating structures.─ Integrative and Comparative Biology; doi:10.1093/icb/icab031.
Tinius, A., Russell, A.P., Jamniczky, H.A. & Anderson, J.S. (2020): Ecomorphological associations of scapulocoracoid form in Greater Antillean Anolis lizards.─ Annals of Anatomy, 231; doi.org/10.1016/j.aanat.2020.151527.
Tinius, A., Russell, A.P. & Jamniczky, H.A. (2021): Geometric morphometry of the breast-shoulder apparatus of Greater Antillean Anolis lizards: in situ investigation of a composite skeletal assemblage and its relationship to ecomorphological categorization.─ Evolutionary Biology; https://doi.org/10.1007/s11692-021-09556-8.
- Shape Variation of the Pectoral Girdle of Anolis Ecomorphs - March 16, 2022
- Morphology of the Scapulocoracoid of Anolis Ecomorphs - September 3, 2020
- Cranial Ornamentation in Anolis baleatus - August 28, 2019
Kevin Aviles
This is very cool! In our study of the morphology of Anolis cristatellus following Hurricane Maria (Aviles-Rodriguez et al. 2021), one of the few changes in pops sampled 4 and 11 months after the hurricane was a widening of the pectoral and pelvic girdles (measured linearly from Xrays), but we were stumped as to how to tie that to a functional trait. It’s cool to learn more about the biomechanics associated with these features.